Transcriptional regulation of cystathionine-γ-lyase in endothelial cells by NADPH oxidase 4-dependent signaling

Journal of Biological Chemistry

Volumn 291, Issue 4, 2016, Pages 1774-1788

  Mistry, Rajesh K ^a   Murray, Thomas V A ^a   Prysyazhna, Oleksandra ^b   Martin, Daniel ^a   Burgoyne, Joseph R ^b   Santos, Celio ^a   Eaton, Philip ^b   Shah, Ajay M ^a   Brewer, Alison C ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD PRESSURE; CELL SIGNALING; CELLS; CYTOLOGY; MAMMALS; PLANTS (BOTANY); TRANSCRIPTION;

CARDIAC MICROVASCULAR ENDOTHELIAL CELLS; HUMAN ENDOTHELIAL CELLS; MOLECULAR SIGNALING; REACTIVE OXYGEN SPECIES; REGULATORY SEQUENCES; TRANSCRIPTIONAL REGULATION; TRANSCRIPTIONAL REGULATOR; TRANSGENIC MICE;

ENDOTHELIAL CELLS;

ACTIVATING TRANSCRIPTION FACTOR 4; CYSTATHIONINE GAMMA LYASE; HYDROGEN SULFIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CELL LOSS; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; C57BL MOUSE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; TRANSGENIC MOUSE; UMBILICAL VEIN ENDOTHELIAL CELL;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; CYSTATHIONINE GAMMA-LYASE; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NADPH OXIDASE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84959037047     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.685578     Document Type: Article

References (58)

1. Aird, W. C. (2007) Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ. Res. 100, 158-173
2. Ignarro, L. J., Buga, G. M., Wood, K. S., Byrns, R. E., and Chaudhuri, G. (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 84, 9265-9269
3. Zakhary, R., Gaine, S. P., Dinerman, J. L., Ruat, M., Flavahan, N. A., and Snyder, S. H. (1996) Heme oxygenase 2: endothelial and neuronal localization and role in endothelium-dependent relaxation. Proc. Natl. Acad. Sci. U.S.A. 93, 795-798
4. Mustafa, A. K., Sikka, G., Gazi, S. K., Steppan, J., Jung, S. M., Bhunia, A. K., Barodka, V. M., Gazi, F. K., Barrow, R. K., Wang, R., Amzel, L. M., Berkowitz, D. E., and Snyder, S. H. (2011) Hydrogen sulfide as endotheliumderived hyperpolarizing factor sulfhydrates potassium channels. Circ. Res. 109, 1259-1268
5. Mustafa, A. K., Gadalla, M. M., and Snyder, S. H. (2009) Signaling by gasotransmitters. Sci. Signal. 2, re2
6. Chiku, T., Padovani, D., Zhu, W., Singh, S., Vitvitsky, V., and Banerjee, R. (2009) H2S biogenesis by human cystathionine γ-lyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. J. Biol. Chem. 284, 11601-11612
7. Yang, G., Wu, L., Jiang, B., Yang, W., Qi, J., Cao, K., Meng, Q., Mustafa, A. K., Mu, W., Zhang, S., Snyder, S. H., and Wang, R. (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase. Science 322, 587-590
8. Wang, M., Guo, Z., and Wang, S. (2012) Cystathionine γ-lyase expression is regulated by exogenous hydrogen peroxide in the mammalian cells. Gene Expr. 15, 235-241
9. Hassan, M. I., Boosen, M., Schaefer, L., Kozlowska, J., Eisel, F., von Knethen, A., Beck, M., Hemeida, R. A., El-Moselhy, M. A., Hamada, F. M., Beck, K. F., and Pfeilschifter, J. (2012) Platelet-derived growth factor-BB induces cystathionineγ-lyase expression in rat mesangial cells via a redoxdependent mechanism. Br. J. Pharmacol. 166, 2231-2242
10. Hughes, M. N., Centelles, M. N., and Moore, K. P. (2009) Making and working with hydrogen sulfide: the chemistry and generation of hydrogen sulfide in vitro and its measurement in vivo: a review. Free Radic. Biol. Med. 47, 1346-1353
11. Lin, V. S., Lippert, A. R., and Chang, C. J. (2013) Cell-trappable fluorescent probes for endogenous hydrogen sulfide signaling and imaging H2O2-dependent H2S production. Proc. Natl. Acad. Sci. U.S.A. 110, 7131-7135
12. Brandes, R. P., Weissmann, N., and Schröder, K. (2014) Redox-mediated signal transduction by cardiovascularNOXNADPHoxidases. J. Mol. Cell. Cardiol. 73, 70-79
13. Burgoyne, J. R., Mongue-Din, H., Eaton, P., and Shah, A. M. (2012) Redox signaling in cardiac physiology and pathology. Circ. Res. 111, 1091-1106
14. Santos, C. X., Anilkumar, N., Zhang, M., Brewer, A. C., and Shah, A. M. (2011) Redox signaling in cardiac myocytes. Free Radic. Biol. Med. 50, 777-793
15. Ray, R., Murdoch, C. E., Wang, M., Santos, C. X., Zhang, M., Alom-Ruiz, S., Anilkumar, N., Ouattara, A., Cave, A. C., Walker, S. J., Grieve, D. J., Charles, R. L., Eaton, P., Brewer, A. C., and Shah, A. M. (2011) Endothelial NOX4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo. Arterioscler. Thromb. Vasc. Biol. 31, 1368-1376
16. Craige, S. M., Chen, K., Pei, Y., Li, C., Huang, X., Chen, C., Shibata, R., Sato, K., Walsh, K., and Keaney, J. F., Jr. (2011) NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation 124, 731-740
17. Schröder, K., Zhang, M., Benkhoff, S., Mieth, A., Pliquett, R., Kosowski, J., Kruse, C., Luedike, P., Michaelis, U. R., Weissmann, N., Dimmeler, S., Shah, A. M., and Brandes, R. P. (2012) Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ. Res. 110, 1217-1225
18. Judkins, C. P., Diep, H., Broughton, B. R., Mast, A. E., Hooker, E. U., Miller, A. A., Selemidis, S., Dusting, G. J., Sobey, C. G., and Drummond, G. R. (2010) Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavailability, and early atherosclerotic plaque formation in apoe-/- mice. Am. J. Physiol. Heart Circ. Physiol. 298, H24-H32
19. Wind, S., Beuerlein, K., Armitage, M. E., Taye, A., Kumar, A. H., Janowitz, D., Neff, C., Shah, A. M., Wingler, K., and Schmidt, H. H. (2010) Oxidative stress and endothelial dysfunction in aortas of aged spontaneously hypertensive rats by Nox1/2 is reversed by NADPH oxidase inhibition. Hypertension 56, 490-497
20. Martyn, K. D., Frederick, L. M., von Loehneysen, K., Dinauer, M. C., and Knaus, U. G. (2006) Functional analysis of nox4 reveals unique characteristics compared to other NADPH oxidases. Cell. Signal. 18, 69-82
21. Hilenski, L. L., Clempus, R. E., Quinn, M. T., Lambeth, J. D., and Griendling, K. K. (2004) Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24, 677-683
22. Murray, T. V., Smyrnias, I., Shah, A. M., and Brewer, A. C. (2013) NADPH oxidase 4 regulates cardiomyocyte differentiation via redox activation of c-jun protein and the cis-regulation of GATA-4 gene transcription. J. Biol. Chem. 288, 15745-15759
23. Brewer, A. C., Murray, T. V., Arno, M., Zhang, M., Anilkumar, N. P., Mann, G. E., and Shah, A. M. (2011) Nox4 regulates nrf2 and glutathione redox in cardiomyocytes in vivo. Free Radic. Biol. Med. 51, 205-215
24. Anilkumar, N., Weber, R., Zhang, M., Brewer, A., and Shah, A. M. (2008) Nox4 and nox2NADPHoxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler. Thromb. Vasc. Biol. 28, 1347-1354
25. Van Buul, J. D., Fernandez-Borja, M., Anthony, E. C., and Hordijk, P. L. (2005) Expression and localization of Nox2 and Nox4 in primary human endothelial cells. Antioxid. Redox Signal. 7, 308-317
26. Dickhout, J. G., Carlisle, R. E., Jerome, D. E., Mohammed-Ali, Z., Jiang, H., Yang, G., Mani, S., Garg, S. K., Banerjee, R., Kaufman, R. J., Maclean, K. N., Wang, R., and Austin, R. C. (2012) Integrated stress response modulates cellular redox state via induction of cystathionine γ-lyase: cross-talk between integrated stress response and thiol metabolism. J. Biol. Chem. 287, 7603-7614
27. Sciarretta, S., Zhai, P., Shao, D., Zablocki, D., Nagarajan, N., Terada, L. S., Volpe, M., and Sadoshima, J. (2013) Activation ofNADPHoxidase 4 in the endoplasmic reticulum promotes cardiomyocyte autophagy and survival during energy stress through the protein kinase rna-activated-like endoplasmic reticulum kinase/eukaryotic initiation factor 2α/activating transcription factor 4 pathway. Circ. Res. 113, 1253-1264
28. Fonseca, S. G., Gromada, J., and Urano, F. (2011) Endoplasmic reticulum stress and pancreatic beta-cell death. Trends Endocrinol. Metab. 22, 266-274
29. Lassot, I., Estrabaud, E., Emiliani, S., Benkirane, M., Benarous, R., and Margottin-Goguet, F. (2005) p300 modulates ATF4 stability and transcriptional activity independently of its acetyltransferase domain. J. Biol. Chem. 280, 41537-41545
30. Lassot, I., Ségéral, E., Berlioz-Torrent, C., Durand, H., Groussin, L., Hai, T., Benarous, R., and Margottin-Goguet, F. (2001) Atf4 degradation relies on a phosphorylation-dependent interaction with the SCF(-TrCP) ubiquitin ligase. Mol. Cell. Biol. 21, 2192-2202
31. Harding, H. P., Zhang, Y., Zeng, H., Novoa, I., Lu, P. D., Calfon, M., Sadri, N., Yun, C., Popko, B., Paules, R., Stojdl, D. F., Bell, J. C., Hettmann, T., Leiden, J. M., and Ron, D. (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633
32. Vattem, K. M., and Wek, R. C. (2004) Reinitiation involving upstream orfs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 101, 11269-11274
33. Diebold, I., Petry, A., Hess, J., and Görlach, A. (2010) The NADPH oxidase subunit nox4 is a new target gene of the hypoxia-inducible factor-1. Mol. Biol. Cell 21, 2087-2096
34. Mittal, M., Roth, M., König, P., Hofmann, S., Dony, E., Goyal, P., Selbitz, A. C., Schermuly, R. T., Ghofrani, H. A., Kwapiszewska, G., Kummer, W., Klepetko, W., Hoda, M. A., Fink, L., Hänze, J., Seeger, W., Grimminger, F., Schmidt, H. H., and Weissmann, N. (2007) Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit nox4 in the pulmonary vasculature. Circ. Res. 101, 258-267
35. Lu, P. D., Harding, H. P., and Ron, D. (2004) Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell biol. 167, 27-33
36. Ron, D. (2002) Translational control in the endoplasmic reticulum stress response. J. Clin. Invest. 110, 1383-1388
37. Petry, A., Djordjevic, T., Weitnauer, M., Kietzmann, T., Hess, J., and Görlach, A. (2006) Nox2 and nox4 mediate proliferative response in endothelial cells. Antioxid. Redox Signal. 8, 1473-1484
38. Lu, L., Han, A. P., and Chen, J. J. (2001) Translation initiation control by heme-regulated eukaryotic initiation factor 2α kinase in erythroid cells under cytoplasmic stresses. Mol. Cell. Biol. 21, 7971-7980
39. Han, J., Back, S. H., Hur, J., Lin, Y. H., Gildersleeve, R., Shan, J., Yuan, C. L., Krokowski, D., Wang, S., Hatzoglou, M., Kilberg, M. S., Sartor, M. A., and Kaufman, R. J. (2013) ER stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 15, 481-490
40. Ameri, K., and Harris, A. L. (2008) Activating transcription factor 4. Int. J. Biochem. Cell Biol. 40, 14-21
41. Enver, T., Brewer, A. C., and Patient, R. K. (1988) Role forDNAreplication in β-globin gene activation. Mol. Cell. Biol. 8, 1301-1308
42. Asimakopoulou, A., Panopoulos, P., Chasapis, C. T., Coletta, C., Zhou, Z., Cirino, G., Giannis, A., Szabo, C., Spyroulias, G. A., and Papapetropoulos, A. (2013) Selectivity of commonly used pharmacological inhibitors for cystathionine β synthase (CBS) and cystathionine γ lyase (CSE). Br. J. Pharmacol. 169, 922-932
43. Shimokawa, H. (2010) Hydrogen peroxide as an endothelium-derived hyperpolarizing factor. Pflugers Arch. 459, 915-922
44. Han, A. P., Yu, C., Lu, L., Fujiwara, Y., Browne, C., Chin, G., Fleming, M., Leboulch, P., Orkin, S. H., and Chen, J. J. (2001) Heme-regulated eif2α kinase (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. EMBO J. 20, 6909-6918
45. McEwen, E., Kedersha, N., Song, B., Scheuner, D., Gilks, N., Han, A., Chen, J. J., Anderson, P., and Kaufman, R. J. (2005) Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J. Biol. Chem. 280, 16925-16933
46. Flora, S. J., Mittal, M., and Mehta, A. (2008) Heavy metal induced oxidative stress its possible reversal by chelation therapy. Indian J. Med. Res. 128, 501-523
47. Brown, S. B., Hatzikonstantinou, H., and Herries, D. G. (1978) The role of peroxide in haem degradation: a study of the oxidation of ferrihaems by hydrogen peroxide. Biochem. J. 174, 901-907
48. Chen, P. F., Tsai, A. L., and Wu, K. K. (1994) Cysteine 184 of endothelial nitric oxide synthase is involved in heme coordination and catalytic activity. J. Biol. Chem. 269, 25062-25066
49. Coletta, C., Papapetropoulos, A., Erdelyi, K., Olah, G., Módis, K., Panopoulos, P., Asimakopoulou, A., Gerö, D., Sharina, I., Martin, E., and Szabo, C. (2012) Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc. Natl. Acad. Sci. U.S.A. 109, 9161-9166
50. Leffler, C. W., Parfenova, H., Jaggar, J. H., and Wang, R. (2006) Carbon monoxide and hydrogen sulfide: gaseous messengers in cerebrovascular circulation. J. Appl. Physiol. 100, 1065-1076
51. Serrander, L., Cartier, L., Bedard, K., Banfi, B., Lardy, B., Plastre, O., Sienkiewicz, A., Fórró, L., Schlegel, W., and Krause, K. H. (2007) Nox4 activity is determined by mrna levels and reveals a unique pattern of ros generation. Biochem. J. 406, 105-114
52. Sciarretta, S., Volpe, M., and Sadoshima, J. (2014) Nox4 regulates autophagy during energy deprivation. Autophagy 10, 699-701
53. Zhang, M., Brewer, A. C., Schröder, K., Santos, C. X., Grieve, D. J., Wang, M., Anilkumar, N., Yu, B., Dong, X., Walker, S. J., Brandes, R. P., and Shah, A. M. (2010)NADPHoxidase-4 mediates protection against chronic loadinduced stress in mouse hearts by enhancing angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 107, 18121-18126
54. Papapetropoulos, A., Pyriochou, A., Altaany, Z., Yang, G., Marazioti, A., Zhou, Z., Jeschke, M. G., Branski, L. K., Herndon, D. N., Wang, R., and Szabó, C. (2009) Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 106, 21972-21977
55. Kolluru, G. K., Shen, X., and Kevil, C. G. (2013) A tale of two gases: no and H2S, foes or friends for life? Redox Biol. 1, 313-318
56. Datla, S. R., Peshavariya, H., Dusting, G. J., Mahadev, K., Goldstein, B. J., and Jiang, F. (2007) Important role of nox4 type NADPH oxidase in angiogenic responses in human microvascular endothelial cells in vitro. Arterioscler. Thromb. Vasc. Biol. 27, 2319-2324
57. Mosharov, E., Cranford, M. R., and Banerjee, R. (2000) The quantitatively important relationship between homocysteine metabolism and glutathione synthesis by the transsulfuration pathway and its regulation by redox changes. Biochemistry 39, 13005-13011
58. Paré, G., Chasman, D. I., Parker, A. N., Zee, R. R., Mälarstig, A., Seedorf, U., Collins, R., Watkins, H., Hamsten, A., Miletich, J. P., and Ridker, P. M. (2009) Novel associations of cps1, mut, nox4, and dpep1 with plasma homocysteine in a healthy population: a genome-wide evaluation of 13 974 participants in the women's genome health study. Circ. Cardiovasc. Genet. 2, 142-150